Querleu 2017
Querleu 2017
Querleu 2017
DOI 10.1245/s10434-017-6031-z
1
Department of Surgery, Institut Bergonié, Bordeaux, France; 2Charles University, Prague, Czech Republic; 3Department
of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY; 4Weill Cornell Medical School, New York, NY
further standardize the anatomic nomenclature, and refine pillar and the mesorectum, medial to the autonomic
the technical descriptions of the different procedures. nerves (Fig. S2), with the goal of preserving bladder
innervation. The medial pararectal space differs from
METHODS the Latzko pararectal space, which is developed
between the rectum medially, the sacrum dorsally,
Anatomic Nomenclature and the internal iliac vessels laterally.
3. The term ‘‘lateral parametrium’’ refers to the parac-
The international anatomic nomenclature can be found ervix. Therefore, we use both terms in this report.
in Terminologia Anatomica (TA)6,7 and should be used Notably, the structure empirically called paracolpos or
wherever it clearly applies. The widely used terms ‘‘ante- paracolpium is included in the paracervix in the TA
rior/posterior,’’ ‘‘deep/superficial,’’ and ‘‘internal/external’’ nomenclature because no border exists between lateral
are confusing. These should be replaced respectively by attachments of the cervix or the vagina. The paracervix
ventral/dorsal, caudal/cranial, and medial/lateral. is a complex structure with a heterogeneous anatomy
The dorsolateral attachment of the cervix is known as that has an impact on surgical management (Figs. 1,
the paracervix. This term should replace numerous other S3). The paracervix contains the main blood and
terms, including ‘‘cardinal ligament’’ or ‘‘Mackenrodt’s lymphatic vessels of the uterine cervix and comprises
ligament’’ (it is not a ligament). However, the term ‘‘me- two parts: the medial part, which is more condensed
sometrium,’’ including the anatomic parametrium and and fibrous, and the lateral part, which is composed of
paracervix, is an accurate correlation with the term ‘‘me- soft lymph node-bearing fatty tissue surrounding
sorectum’’ (used in rectal cancer surgery) because it refers vessels and nerves. The most stable anatomic land-
to the area at risk for discontinuous spread of cervical mark delineating the boundary between the two parts is
carcinoma. It has been associated with a functional view of the distal ureter (Fig. S1). The deep uterine vein
cancer spread based on embryologic development, a con- invariably runs cranial and perpendicular to the
cept that deserves consideration but remains hypothetical.8 hypogastric plexus (Fig. 2). However, the number of
Strict use of TA nomenclature is not necessarily appli- uterine veins may vary, and the deep uterine vein does
cable in surgical practice, in which different structures are not exactly represent the caudal limit of the paracervix.
created by surgical dissection and separated by artificially Figure 2 shows cellular paracervical tissue caudal to
created spaces. We describe these as follows: the deep uterine vein. The node-bearing tissue of the
lateral part of the paracervix can be removed with
1. The ‘‘ventral parametrium’’ is defined after surgical
preservation of the vessels and nerves as in any lymph
opening and development of two surgical spaces: the
node dissection. As stated by Palfalvi and Ungar,11
vesicouterine and vesicovaginal septum medially and
‘‘the border between parametrial dissection and lym-
the medial paravesical space laterally. The medial
phadenectomy is artificial and can be located in
paravesical space is developed medial to the lateral
ligament of the bladder, which contains the umbilical
and superior vesical arteries (Fig. S1). The medial
vesical space differs from the lateral (Latzko) par-
avesical space, which is developed between the
umbilical ligament and the external iliac vessels. The
ventral parametrium can be surgically divided into two
portions: one in the plane medial to the terminal ureter
(vesicouterine ligament cranial to the ureter and
vesicovaginal ligament caudal to the ureter) and the
other lateral to the plane of the ureter. The bladder
nerves run caudally and parallel to the ureter. Some
Japanese authors refer to the vesicovaginal ligament as
the ‘‘posterior leaf of the vesicouterine ligament.’’9
2. The ‘‘dorsal parametrium’’ is a complex structure
composed of the rectouterine and rectovaginal liga-
Deep uterine vein Inferior
ments (rectal pillar) and the dorsal part of the pelvic hypogastric plexus
autonomic nerves. A medial pararectal space (other-
wise described as the sacrouterine space or Okabayashi FIG. 1 Paracervix showing deep uterine vein and inferior hypogas-
space10) can be artificially created lateral to the rectal tric plexus. Courtesy of Dr. Ghislaine Escourrou, University Hospital,
Toulouse, France
Querleu–Morrow Classification: Hysterectomy
B2
Inferior hypogastric
plexus
A
B
D
Ureter
Updating Process
visualization (after opening of the ureteral tunnels) at the resection. Approximately 10 mm of the vagina from the
time of abdominal or laparoscopic surgery or by palpation caudal edge of the cervix or tumor is resected, without
at the time of vaginal surgery. The uterine pedicles can be intent to radically resect the paravaginal tissues. The
transected at their crossing with the ureter, as in the orig- vesicovaginal ligament is not resected. As a result, the
inal Wertheim operation, or at their origin. The paracervix bladder nerves, which run within the vesicovaginal liga-
is transected medial to the ureter but lateral to the cervix. ment caudal to the ureter and lateral to the vaginal fornix,
The paracervix is excised halfway between the ureter and are not at risk. The radicality of this operation can be
the cervix and caudally parallel to the cervix until the increased without increasing the risk of hypogastric nerve
lateral vaginal fornix is reached and opened. Kinking or injury.
thermal injury of the distal ureter (related to the en bloc use Although the type B1 procedure does not involve
of heat-generating devices) is a concern because the ureter resecting the nodes of the lateral part of the paracervix, a
is not fully mobilized. The rectovaginal ligaments and the paracervical lymphadenectomy can be added to increase the
vesicouterine ligaments are defined, then divided at a dis- radicality of node dissection. This results in a type B2
tance from the uterus, but not at the rectum or bladder. This resection. Combined with pelvic lymphadenectomy, type
involves an approximate 5-mm resection of the corre- B2 surgeries aim to remove the pelvic nodes as completely
sponding ligaments. No removal of the vaginal part of the as possible. In this context, resection of the nodes located
paracervix (paracolpos) is involved. Vaginal resection is caudal to the obturator nerve and cranial to the sciatic nerve
minimal, routinely less than 10 mm. is part of the additional paracervical lymphadenectomy.
Obtaining a free exocervical margin without any inva- Adding a lateral paracervical nodal dissection to a
sive or preinvasive disease is a major objective of surgery proximal-type radical hysterectomy improves lateral radi-
in the setting of early cervical cancer. Although colpec- cality without increasing morbidity.8,12,13 The gluteal and
tomy may constitute overtreatment in some cases, without pudendal nodes, which are caudal and lateral to the iliac
it there is a risk of involved margins or even incomplete vessels, are included in the template. The procedure may be
resection of the cervical stroma. However, patients with refined by the use of indocyanine green navigation, which
preoperative in sano cone biopsy could be spared allows the surgeon to identify the lymph vessel and lymph
colpectomy. node component of the paracervix more clearly.15
Our goal is to define a new surgical option (i.e., ‘‘min- The goal is to incorporate recent developments associ-
imal radical surgery’’), which is a smaller operation than ated with the use of ICG navigation, as published by others.
the standard modified radical hysterectomy (type B, We do not take sides in this regard because our objective is
described in the next section), but a larger operation than a to make the proposed classification system adaptable to
simple or extrafascial hysterectomy/trachelectomy. In recent surgical variations.
general, we do not recommend any specific type of surgical
radicality for every clinical situation. Although the trend Type C: Transection of the Paracervix at Its Junction
toward conservative surgery in the setting of early cervical with the Internal Iliac Vascular System This operation
cancer may be justified, to date, no definitive evidence corresponds to the classical radical hysterectomy. It is
ensures that ‘‘simple’’ procedures are safe. Furthermore, we adapted to International Federation of Gynecology and
are concerned about disseminating the idea that early cer- Obstetrics (FIGO) stage IB1 lesions with deep stromal
vical cancer can be managed using a common, non-radical invasion and IB2-2A or early 2B cervical cancers. The
procedure. We fear that this may lead to suboptimal lateral border is defined as the medial aspect of the internal
surgeries without adequate preoperative staging in non- iliac artery and vein.
specialized settings. Transection of the rectovaginal and rectouterine liga-
ments is performed at the rectum. Transection of the
Type B: Resection of the Paracervix at the Ureter This ventral parametrium ligament is performed at the bladder.
operation (Figs. 4, S4) includes two subtypes: types B1 and Both the vesicouterine and vesicovaginal ligaments are
B2. Type B1 is the ‘‘modified’’ radical hysterectomy. The resected. The ureter is completely mobilized and lateral-
ureter is unroofed and mobilized laterally, permitting ized. The length of the vaginal cuff is adjusted to the
transection of the paracervix at the level of the ureteral vaginal extent of the tumor.
tunnel. In type C procedures, the decision about autonomic
The caudal limit must not involve the inferior nerve preservation is crucial. Two subcategories are
hypogastric plexus (Fig. S4). Partial resection of the uter- defined in the following sections.
osacral peritoneal fold of the rectouterine ligament (dorsal
parametrium) and the vesicouterine (ventral parametrium) Type C1: Nerve-preserving Radical Hysterectomy The
ligament also is a standard component of this dorsal parametrium is transected after the dorsal segment
Querleu–Morrow Classification: Hysterectomy
of the autonomic nerve system has been separated Höckel.16 It usually is performed for laterally recurrent
(Fig. S2). The inferior hypogastric plexus is systematically tumors as a separate procedure.
identified and preserved by transecting only the uterine Table 1 defines the different classes of radical
branches of the pelvic plexus at the time the lateral para- hysterectomy.
metrium is transected. Ventrally, the bladder branches of
the pelvic plexus are preserved in the vesicovaginal liga- DISCUSSION
ment. Then, only the medial part of the ventral
parametrium is resected, and the bladder branches of the The popular Piver–Rutledge–Smith classification,17
hypogastric plexus caudal to the course of the ureter are published in 1974, describes five classes of radical hys-
identified and preserved. terectomy. The original paper does not refer to clear
anatomic landmarks and international anatomic definitions.
Type C2: No Preservation of Autonomic Nerves The Excessive vaginal resections, from one third to three
paracervix is completely transected. The inferior fourths of the vagina, are included in some templates. Class
hypogastric plexus, together with the sacral splanchnic 1 is not a radical hysterectomy, and class 5 is no longer
nerves, is divided lateral to the rectum. Type C2 requires a used. The rationale and anatomy differentiating classes 3
complete dissection of the ureter from the ventral and 4 are not clear. Finally, the Piver–Rutledge–Smith
parametria (vesicovaginal ligament). The ventral parame- classification applies only to open surgery and was devel-
tria are resected at the level of the bladder wall (Fig. S5). oped at a time when minimally invasive and fertility-
Bladder branches of the hypogastric plexus are sacrificed, sparing operations did not exist. It fails to take into account
so it is not necessary to identify them. Laterally, the the concept of nerve preservation and ignores the vaginal
resection continues alongside the medial aspect of the approach.
internal iliac vessels down to the pelvic floor. An interesting tumor-node-metastasis (TNM)-like
The medial pararectal (sacrouterine), lateral pararectal, description of the operation that defines three classes of
and lateral paravesical spaces are unified by transecting the radicality in all directions has been developed.18 However,
pelvic attachment of the paracervix together with the the model results in 91 possible subtypes.
splanchnic nerves in the caudal part (Fig. S6). Parts of the Two metrics define the outcomes of radical hysterec-
vaginal component of the paracervix (paracolpium) are tomy: (1) adverse effects such as bladder and rectal
removed. The removal of the dorsal parametrium is dysfunction and (2) the curative effect of the surgery.
extended caudally to the sacral attachment. The more extensive the surgery is, the higher the risk of
Type C is the standard operation for bulky or high-risk complications. However, small surgeries may undertreat
tumors. Type C1 has become the mainstay. Type C2 can be high-risk tumors, whereas big surgeries may overtreat
justified only for anatomic reasons. low-risk tumors. The Querleu–Morrow classification
provides a simple and universal tool for assigning dif-
Type D: Laterally Extended Resection These less ferent levels of radicality to a limited number of
common surgeries feature additional ultra-radical categories. Some surgeries may be asymmetric. The
procedures, in which structures lateral to the paracervix same classification applies to fertility-sparing surgeries
are resected. Two subtypes are described in the following (type B, as in the Dargent operation, and type A in new
sections. variants adapted to minimal disease or after neoadjuvant
Type D1: Resection of the Entire Paracervix at the chemotherapy).
Pelvic Sidewall Together With the Hypogastric and Because it is impossible to describe all variations of
Obturator Vessels, Exposing the Roots of the Sciatic these procedures, the use of a simple classification system
Nerve. The resection plane is lateral to the internal iliac does not preclude a careful description of any single
vessels, interrupting branches of gluteal superior, gluteal operation. The list of required information should be a
inferior, and pudendal vessels. This procedure corresponds component of quality control in the surgical management
to the Palfalvi–Ungar laterally extended parametrectomy11 of cervical cancers. The following items should appear in
and may be used for stage 2B tumors. the operative report:
Type D2: D1 Plus Resection of the Adjacent Fascial/
• All components defining the type of radical hysterec-
Muscular Structures. These structures include, when nec-
tomy. The management of the lateral, ventral, and
essary, the obturator fascia and obturator muscle ventrally,
dorsal attachments of the cervix must be described.
the coccygeus muscle and pelvic part of the piriformis
• Mode of management of the uterine artery, which is
muscle dorsally, and the sacrospinous ligament and
routinely divided at its origin from the internal iliac
acetabulum laterally. This procedure corresponds to the
artery but may be divided at the ureter in type A
laterally extended endopelvic resection described by
D. Querleu et al.
TABLE 1 Summary of the main landmarks in each type of radical hysterectomy on each part of the parametria
Dimension Paracervix or lateral parametrium Ventral parametrium Dorsal parametrium
Type of
radical
hysterectomy
A Halfway between the cervix and ureter Minimal excision Minimal excision
(medial to the ureter–ureter identified
but not mobilized)
B1 At the ureter (at the level of the ureteral Partial excision of the vesicouterine ligament Partial resection of the
bed–ureter mobilized from the cervix rectouterine-rectovaginal
and lateral parametrium) ligament and uterosacral
peritoneal fold
B2 Identical to B1 plus paracervical Partial excision of the vesicouterine ligament Partial resection of the
lymphadenectomy without resection rectouterine-rectovaginal
of vascular/nerve structures ligament and uterosacral fold
C1 At the iliac vessels transversally, caudal Excision of the vesicouterine ligament at the At the rectum (hypogastric nerve
part is preserved bladder. Proximal part of the vesicovaginal is dissected and spared)
ligament (bladder nerves are dissected and
spared)
C2 At the level of the medial aspect of iliac At the bladder (bladder nerves are sacrificed) At the sacrum (hypogastric nerve
vessels completely (including the is sacrificed)
caudal part)
D At the pelvic wall, including resection At the bladder. Not applicable if part of exenteration At the sacrum. Not applicable if
of the internal iliac vessels and/or part of exenteration
components of the pelvic sidewall
These studies suggest that the risk of visceral lymph node descriptions and nomenclature of the fasciae and ligaments of the
involvement is associated with tumor size and stage, female pelvis: a dissection-based comparative study. Am J Obstet
Gynecol. 2005;193:1565–73.
clearly supporting the concept that the extent of excision 8. Höckel M, Horn LC, Fritsch H. Association between the mes-
should increase, or widen, as stage and tumor size increase. enchymal compartment of uterovaginal organogenesis and local
However, both studies were based on specimens derived tumor spread in stage IB-IIB cervical carcinoma: a prospective
from type C operations. Neither study was designed to study. Lancet Oncol. 2005;6:751–6.
9. Fujii S, Tanakura K, Matsumura N, Higuchi T, Yura S, Mandai
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risk cervical cancers. radical hysterectomy. Gynecol Oncol. 2007;104:186–91.
Our proposed classification is not a guideline, but rather 10. Yabuki Y, Asamoto A, Hoshiba T, Nishimoto H, Satou N. A new
a standardized description of different surgeries performed proposal for radical hysterectomy. Gynecol Oncol.
1996;62:370–8.
worldwide, independent of underlying theoretical objec- 11. Palfalvi L, Ungar L. Laterally extended parametrectomy (LEP),
tives or the surgeon’s choice of approach in individual the technique for radical pelvic sidewall dissection: feasibility,
cases. Two major objectives are constant: (1) excision of technique, and results. Int J Gynecol Cancer. 2003;13:914–7.
the central tumor with clear margins and (2) removal of any 12. Höckel M, Konerding MA, Heussel CP. Liposuction-assisted
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potential site of node metastasis. Future randomized studies nale, surgical anatomy, and feasibility study. Am J Obstet
designed to document the need for extended or reduced Gynecol. 1998;178:971–6.
radicality in the surgical management of cervical cancer 13. Querleu D, Narducci F, Poulard V, Lacaze S, Occelli B, Leblanc
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ACKNOWLEDGEMENT This study was funded in part through radical trachelectomy: a novel concept to preserve uterine bran-
the NIH/NCI Support Grant P30 CA008748 (Nadeem R. Abu- ches of pelvic nerves. Eur J Obstet Gynecol Reprod Biol.
Rustum). 2015;193:5–9.
15. Kimmig R, Aktas B, Buderath P, Rusch P, Heubner M. Intra-
DISCLOSURE Denis Querleu received travel expenses for the operative navigation in robotically assisted compartmental
2014 IGCS meeting (Melbourne) from Karl Storz GmBH. He has surgery of uterine cancer by visualisation of embryologically
consulted for Roche Inc. Other authors declares no conflicts of derived lymphatic networks with indocyanine-green (ICG). J
interest. Surg Oncol. 2016;113:554–9.
16. Höckel M. Laterally extended endopelvic resection: surgical
treatment of infrailiac pelvic wall recurrences of gynecologic
malignancies. Am J Obstet Gynecol. 1999;180:306–12.
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